PSYCHOLOGICAL REVIEW
VOL. 78, No. 6 NOVEMBER 1971
SPECIFIC HUNGERS AND POISON AVOIDANCE AS ADAPTIVE SPECIALIZATIONS OF LEARNING1
PAUL ROZIN 2 AND JAMES W. KALAT3 University of Pennsylvania
Learning and memory are considered within an adaptive-evolutionary frame- work. This viewpoint is illustrated by an analysis of the role of learning in thiaraine specific hunger. Consideration of the demands the environment makes on the rat and the contingencies it faces in the natural environment, appreciation of the importance of the novelty-familiarity dimension for these animals, and the realization of two new principles of learning, permit a learning explanation of most specific hungers. The two new principles, "belongingness" and "long-delay learning" specifically meet the peculiar demands of learning in the feeding system. In conjunction with the importance of the novelty dimension, they are discussed in an attempt to develop the laws of taste-aversion learning. It is argued that the laws or mechanism of learning are adapted to deal with particular types of problems and can be fully under- stood only in a naturalistic context. The "laws" of learning in the feeding system need not be the same as those in other systems; manifestation of a learning capacity in one area of behavior does not imply that it will be acces- sible in other areas. This notion leads to speculations concerning the evolution and development of learning abilities and cognitive function. Full under- standing of learning and memory involves explanation of their diversity as welLas the extraction of common general principles.
The application of the basic principles developed in situations and species where of evolution and adaptation to learning other solutions to the problems at hand and memory offers a hopeful means of arc less adaptive. Furthermore, when conceptualizing and ordering the increas- learning or memory capacities are brought ingly diverse data of these fields. Learning to bear on a particular type of problem or and memory, being the result of natura situation, it stands to reason that these selection, should be expected to be best capacities should be shaped by or adapted to the situation. 1 This manuscript is an expanded version of an We propose to treat learning and invited address by the first author to APA Division memory as any Other biological char- 6 in 1969. The preparation of this article and some ^ • ,.• i • 4. 4. 4 i i ., • j of the research reported in it were supported by actenstic, subject to natural selection and National Science Foundation Grant GB 8013. We therefore adapted to handle specific types would like to thank John Garcia, Henry and Lila of problems. Insofar as an important Gleitman Elisabeth Rozin, Martin SeligmanW. J. environmental problem (e.g., obtaining Smith, and Richard Solomon for their helpful com- f , -. . , , ments and criticisms. adequate foods) presents unique demands 2 Requests for reprints should be sent to Paul or contingencies, we would expect to find Rozin, Department of Psychology, University of appropriate modifications of learning and Pennsylvania, Philadelphia, Pennsylvania 19104. •!•.• 1 1 i ^ j -^i 'Supported by National Institute of Health memory abilitiesL , closely articulated with training grant. Now at Duke University. one another and with the natural behavior 459 © 1971 by the American Psychological Association, Inc. 460 PAUL ROZIN AND JAMES W. KALAT of the organism. Biologically speaking, significant part of our understanding of there is no reason to assume that there sensory psychology and physiology. Spe- should exist an extensive set of generally cializations in sensory function, as shown applicable laws of learning, independent of in the classic works of Lettvin, Maturana, the situation in which they are manifested. McCulloch, and Pitts (1959) in the visual This is not to say that there might not be system of the frog, Capranica (1966) on some general laws, at a minimum resulting the remarkable tuning of the frog auditory from basic constraints and features of the system to mating calls, and Roeder (1963) operation of the nervous system, and perhaps reflecting general principles of on detection of bat sonar by the moth causality in the physical world. However, auditory system, can be fully understood if we look at learning within an adaptive- only in the context of adaptations to evolutionary framework, we should seek natural problems. The incredible diversity not only to uncover some of the greatest of the visual system (e. g., variations in the common denominators among the be- proportion of rods and cones in the retina haviors we study, but also to explore the as a function of species and ecology) can plasticity of the mechanisms themselves, be ordered and comprehended in a phy- as they are shaped through selection to logenetic adaptive framework, as shown deal with particular types of problems. in the classical work of Walls (1942). We For many years, the leading ethologists would like to suggest that there are similar (e.g., Lorenz, 1965; Tinbergen, 1951) have possibilities in the area of learning and espoused a position consistent with this. memory. They have emphasized the importance of considering learning within a naturalistic In the major portion of this paper, we context; learning is viewed as being shall discuss specific hungers and poisoning genetically programmed to occur at specific in rats. We shall argue that some basic points in an ongoing behavior sequence. features of learning and memory as applied The thesis presented here is in harmony to food selection in the rat are strikingly with the ethologists' position, but em- different from features characterizing the phasizes differences in learning mechanisms rat's learning in more traditional laboratory themselves, as a function of the situations situations, that these differences make in which learning occurs. sense in terms of evolutionary adaptation, In the face of recent evidence, coming and that an understanding of the role of most significantly from the work of Garcia learning and memory in food selection in- and his colleagues (Garcia, Ervin, & volves an elucidation of specifically adapted Koelling, 1966; Garcia & Koelling, 1966), learning mechanisms and an integration challenging two important generalities in of these with genetically determined be- learning, a framework for ordering the havior patterns. suggested diversity of laws of learning is In the remaining portion of the paper, we desirable. We propose such a framework in terms of the notion of adaptive specializa- shall discuss whether the feeding system tions. Consideration of learning from the is a unique case or representative example, adaptive point of view offers two ad- relate our position to somewhat similar vantages: (a) it provides a heuristic, for theoretical positions, including ethology ordering and predicting the types of learn- and the recent papers of Garcia (Garcia & ing one will see in different situations, and Ervin, 1968; Garcia, McGowan, & Green, (b) it provides a type of explanation of be- 1971), Revusky (Revusky, in press; Re- havior, in that one aspect of understanding vusky & Garcia, 1970), Seligman (1970), behavior can be considered to be explica- Lockard (1971), and Shettleworth (1971), tion of its adaptive value. and discuss the implications of our position Adaptive considerations have proved in the areas of comparative psychology of useful in many areas of biology and are a learning and human function. ADAPTIVE SPECIALIZATIONS OF LEARNING 461
SPECIFIC HUNGERS learning had to be involved. This served Basic Phenomenon and Problems with a as the impetus for our investigation of Learning Interpretation specific hungers. The first demonstration of vitamin B The phenomena of specific hungers were hunger was that of Harris et al. (1933), beautifully demonstrated in the classical who found that given a choice of three work of Richter (1943). The question foods, one supplemented with B vitamins, raised by this work was, How is the animal B vitamin deficient rats would quickly (in particular, the rat) able, when deficient come to choose the correct food. For in a particular nutrient, to select those convenience, Rozin, Wells, and Mayer foods containing it? In the case of sodium, (1964) decided to study a more simplified it is quite clear that sodium deficiency re- situation. One vitamin, thiamine, was leases an innate preference for substances selected, since a clear specific hunger for containing sodium (Nachman 1962; Rich- thiamine had been reported (Richter, ter, 1956; Strieker & Wilson, 1970). How- Holt, & Barelare, 1937; Scott & Quint, ever, it is hard to believe that the rat comes 1946). The most pronounced symptoms equipped with prewired recognition systems of thiamine deficiency in the rat are weight for each of the many substances for which loss and anorexia. (More details about this it can show a specific hunger. The al- and other aspects of thiamine hunger are ternative view holds that rats can learn available in a review by Rozin, 1967a). about what foods "make them better" Following injection or ingestion of thiamine, when they are ill and in this manner come deficient rats show clear signs of reversal to select the proper nutrients (Harris, of symptoms within a few hours, at most. Clay, Hargreaves, & Ward, 1933; Scott The basic design consisted of raising wean- & Quint, 1946). Rats would, in their ling rats on a thiamine deficient diet for lifetime, learn preferences for the tastes of 21 days, at which point they showed clear only those foods associated with recovery signs of deficiency. At this point they from the deficiencies they happen to have were offered a choice between this deficient experienced. This notion has the distinct diet and the same diet supplemented with advantage of simplicity in that it accounts thiamine. for all of the specific hungers (except sodi- Thiamine deficient animals strongly pre- um) with one basic mechanism. ferred the thiamine enriched choice, while There was, in fact, some evidence for a control animals who were not deficient, but learning interpretation of specific hungers. otherwise treated identically, did not. A Scott and Verney (1947) offered a dis- few rats with a choice between deficient tinctively flavored vitamin supplemented and highly enriched diet showed no clear food and an unflavored deficient food to preference during the first few choice days, deficient rats. After a preference developed but in the meantime ingested great amounts for flavored, enriched food, the flavor was of thiamine and showed marked recovery. switched to the deficient food. By and Subsequently, these rats developed a clear large, rats now preferred the flavored defi- preference for the thiamine rich diet. It cientfood, suggestinga learning mechanism. seemed highly unlikely that a rat would The problem with a learning interpreta- show a preference for what it would have tion, so far as psychologists were concerned, needed a few days ago without showing was the long delay of reinforcement. The that same preference when the thiamine recovery (reward) effects produced by an presumably had reinforcing value. This ingested nutrient would not occur until anomalous observation was confirmed in an many minutes or hours after ingestion. experiment in which rats were made This poses serious problems for a learning deficient in thiamine and then recovered mechanism within the context of traditional from deficiency by injection of high learning theory. If specific hungers were amounts of thiamine while consuming the in fact learned, then some new type of deficient diet. After a period of recovery, 462 PAUL ROZIN AND JAMES W. KALAT the rats were offered a choice of thiamine Reinterpretation of Specific Hungers enriched and deficient diets. Preferences for the thiamine enriched diets in rats that The first step in the resolution of the had been deficient emerged at all the re- problem as formulated came with the covery intervals studied (Rozin, 1965). appreciation of the importance of novelty This result raises a second problem for a in the determination of food preferences learning interpretation of thiamine hunger: in deficient rats (Rodgers & Rozin, 1966). How could rats develop a learned prefer- Deficient rats show an immediate and ence for something that at the time the almost complete preference for new foods, preference appeared, had no known rein- even when the new food is thiamine forcing effects? If the preference developed deficient and the old food has a thiamine because of the initial reinforcing effects supplement. In this case, the new-food of the thiamine, why did it not appear preference reverses after a few days. The suggested until much later? We shall call this results that the "specific hunger" problem Preference after recovery. for thiamine may be simply a reflection of Careful consideration of the specific the thiamine deficient rat's preference for hungers situation and contingencies gave new foods: If the new food contains rise to additional problems that could not thiamine, a learned preference could de- be easily solved within the traditional learn- velop (mechanism still unknown). ing framework. Given that a rat might Rodgers (1967a) succeeded in demon- learn with the delays of reinforcement that strating quite conclusively that there is no seem to hold here, how would the recovery specificity to thiamine specific hunger. be specifically associated with a particular Reasoning that the novelty response might food? If the animal had eaten from a overwhelm an existing tendency to prefer number of the choices available (or both the vitamin, Rodgers offered deficient rats choices in the two-choice situation), how the choice of a deficient novel diet or the could one of these choices, presumably the same novel diet supplemented with thi- one containing thiamine, show a specific amine. The usual strong specific hunger increase in preference? In other words, did not appear. Furthermore, when the if an ingestion of two or more foods is choice was between two different novel followed by recovery, how does one of these diets, one enriched, preferences for the foods acquire positive properties? We enriched source did not develop rapidly. shall call this third problem, Which food? Finally, separate groups of thiamine defi- A logical extension of this notion raises cient rats and pyridoxine deficient rats the question of how food or the eating of were offered their basal diet in two forms: food becomes associated with recovery one supplemented with thiamine, the other when many other potential candidates for with pyridoxine. If there were any spe- association exist in the environment. After cificity, one would expect each group to all, following ingestion of foods including show a preference for the vitamin that the vitamin enriched food, and before would produce recovery. There were no recovery can ensue, the rat performs many significant differences between the groups. acts, such as chewing, grooming, exploring, There seemed to be two types of ex- and sleeping, and receives many stimuli. planations for the novelty effect. One is By what principle does he elect to respond that the deficiency experience triggers an to food stimuli instead of other stimuli? innately programmed "neophilia." A more We call this fourth problem, Why food? attractive hypothesis is that the novelty We have, then, four problems in the effect comes about through learning. The application of traditional learning principles paradigms described all pit the new food to the explanation of specific hungers: against the familiar food that has been associated with deficiency. The new-food 1. Delay. preference could be a reflection of an 2. Preference after recovery. aversion to the old food. Put more col- 3. Which food? loquially, we could ask whether preferences 4. Why food ? for new foods appear because the rat ADAPTIVE SPECIALIZATIONS OF LEARNING 463
"loves the nev stuff or hates the old of recovery, and after a 16-hour period of stuff." The i:ssue can be clarified by food deprivation, they were presented again watching the behavior of deficient animals with the familiar deficient food for the toward different foods (Rozin, 1967b). first time since the onset of recovery. These Rats housed in relatively large individual food deprived rats, showing no signs of cages were observed during the first 15 deficiency at this time, responded to the minutes of an 8-hour food presentation familiar deficient food as they had before, each day. The r responses were classified with minimal ingestion and occasional into a number of categories, such as groom- spillage and redirected feeding. In this ing, sleeping, eating, and chewing. The case, a "normal" hungry rat prefers staying experimental ;ts were placed on a thi- hungry to eating its original diet which amine deficient diet. As deficiency de- provides, in fact, perfectly adequate nutri- veloped, less time was spent eating during tion for him at the time, and is normally the first 15 mirutes, and two striking be- quite palatable. Preference of hunger haviors, quite :-are in normals, appeared. (eating nothing) to ingestion in hungry One was spillag< of the food: the rat would rats and the similarity in the rat's be- approach the food cup, sniff at the food, havior toward deficient and highly un- and then paw at the food in a scooping palatable (quinine adulterated) diets sug- motion, spilling it out of the cup, so that gests strongly that we are dealing with an it fell through l[he wire mesh floor. (This aversion to the familiar food. spillage phenon.enon in deficient rats was The learned aversion interpretation actually quite familiar, since we have places specific hungers in a new perspec- always had some difficulty measuring the tive. We can consider the deficient diet food intake of deficient rats on this ac- as a CS and the nausea or other ill effects count.) The otaer new behavior was what produced by its ingestion as a UCS. we call "redire :ted feeding." Following Presumably, the classically conditioned this initial investigation of the food cup, "ill effects" lead to avoidance of the rats would occasionally move over to the familiar food. The mechanism suggested wooden barrier separating the nest area for the specific hunger phenomenon, as from the rest of | the cage and begin to chew seen in the standard two-diet choice, would it vigorously. iThey would also, occasion- then be that the rat learns an aversion to ally, chew on the cage wires. These two the familiar deficient food. Before the behaviors suggested an aversion to the time of choice, he has already done a most familiar diet. The redirected feeding sug- significant part of his learning: He knows gests conflict between desire to eat and what not to eat. The initial preference the aversiveness of the food offered. for the new food follows. Its maintenance Spillage is often seen in normal rats with when the new food is enriched could be highly unpalatable foods, such as quinine accounted for as an additional learned adulterated diet 3. preference for the new food or as a failure When offered! the old deficient food in a to develop an aversion to it (see section new container (metal instead of glass) in on learned preference). a new location, (these deficient rats showed To the extent that specific aversions little potentiati
has to do with the variable environment. tion are not what they were thought to be. In the face of a changing and variable en- (b) The novelty-familiarity dimension is vironment, it would be maladaptive to pro- of particular importance to the rat. (c) gram specific modes of response, since these To account fully for the phenomenon, two would often be inappropriate. Clearly, a new "principles" of learning were needed: plastic organism can do better in a plastic belongingness and long delay. It is re- environment. (We expect that mono- markable that each of Garcia et al.'s two phagous animals are less capable of learn- "classic" experiments (Garcia & Koelling, ing about food than omnivorous ones.) 1966; Garcia et al., 1966) dealt directly The second factor predisposing to learning with one of these problems at just the time has to do with the "cost of preprogram- that these two issues became the two prob- ming." This has two components. First, lems in specific hungers. preprogramming of a particular behavior or In the context of the problems of specific stimulus configuration preempts a portion hungers, it seemed clear that the basic of the total genetic material, which could principles demonstrated in these experi- otherwise be used for some other purpose. ments must be essentially correct. Both Second, there may be greater costs as- principles, belongingness and long-delay sociated with the evolution of genetic- learning, seem highly adapted to the pro- ally programmed solutions, insofar as perties of the feeding system. Tastes are built-in solutions involve more genetic in fact causally linked to gastrointestinal reorganization. events, and there is a long inherent delay Of course, in some cases, a genetically between the taste and its consequences. programmed recognition may be replaced We suggest that specific learning mech- by a learning mechanism. If an animal anisms have evolved in response to specific had the capability of learning something problems. In the following section, we that was genetically programmed, other- shall consider taste-aversion learning in wise favorable mutations in the genetic greater detail, in order to demonstrate the material responsible for this behavior could extensive ways in which learning mech- be selected for, even though the genetic anisms may be modified to satisfy particular basis for the behavior would be destroyed. demands. Given a general learning capability, it could often be cheaper to allow the en- TASTE-AVERSION LEARNING: AN vironment to supply the appropriate stimu- EXAMPLE OF ADAPTIVE SPECIAL- lus configurations, even if these will not IZATION OF LEARNING vary much throughout life. We suggest that this "balance sheet" type of approach In this section we shall consider learning may be fruitfully applied to all specific about food. In considering whether it is a hungers. In the case of the chick, we sug- "new type" of learning, we shall examine gest that it is necessary to genetically both the belongingness and delay principles specify those portions of the feeding and in some detail, consider the importance of drinking system which are distinctively familiarity and novelty, and explore other different (the ingestive responses and possible differences between learning in regulation). Since the chick's behavior the feeding system and more traditional leads to water in the beak anyway, be- types of learning. cause the preprogrammed food recognition overlaps with this aspect of drinking, a Principles of Stimulus Selection cheap way out can be found. The costs can presume, from the material on are minimal, and the genetic savings, specific hungers, that when faced with a significant. bewildering array of stimuli as candidates SUMMARY for association with a gastrointestinal The reanalysis of specific hungers rests event, the rat has available principles with on three fundamental points: (a) The which to sort them out. One concerns his actual contingencies in the feeding situa- past experience with these stimuli, the ADAPTIVE SPECIALIZATIONS OF LEARNING 471
novelty-familiarity dimension, and the substances to eat and which to avoid. other certain presumably built-in tend- However, an equal ability to associate encies to associate certain categories of lights and sounds with gastrointestinal stimuli with certain relevant events (be- consequences would be far less adaptive; longingness). We shall consider each in in fact, the common result would be turn. "superstitious" learning. The belonging- ness phenomenon receives support not only Novelty-Familiarity Dimension and from these adaptive arguments but also As sociability from neurological considerations. The gustatory receptors and the gut receptors We have argued that the novelty (or are similarly classified as visceral sensory familiarity) of a stimulus is of particular inputs and show close neurological re- importance for a rat (see Galef, 1970; lationships, specifically in the medulla and Rozin, 1968). This distinction has par- possibly in the hypothalamus. ticular significance in determining the It appears that under some circum- magnitude of a learned aversion to a given stances, exteroceptive cues can become as- taste. Revusky and Bedarf (1967) and sociated with poisoning (Garcia, Kimel- Wittlin and Brookshire (1968) showed that dorf, & Hunt, 1961; Rozin, 1969b). rats learn aversions much more readily to Rather rapid learning of aversion to loca- novel than to familiar solutions, even when tions and shape of drinking vessel can be the familiar solution is drunk after the demonstrated if the UCS (apomorphine) novel solution (and, of course, before is introduced during drinking from the poisoning). In these experiments, familiar- appropriate vessel (Rozin, 1969b). On the ization occurred over a period of days, but, other hand, even with a modest 30-minute in fact, a 20-minute exposure to a solution CS-UCS interval and the use of a con- followed by neutral consequences will pro- catenation of nontaste cues including duce virtually the same effect, for such a vessel shape, location, solution texture, and solution is then quite resistant to associa- 6 temperature, virtually no aversion appears tion with poisoning (Kalat & Rozin ). after many trials (Rozin, 1969; but see This minimal (single) experience can have Nachman, 1970a, for a demonstration that occurred three weeks before the poisoning under proper circumstances oral tempera- without significant attenuation of the ture—a nontaste but interoceptive cue— effect. alone may be an effective cue). The sug- gestion here is that at least part of the Belongingness "weakness" of exteroceptive cues derives The "belongingness" (Garcia & Koelling, from a very rapid decay of their associ- 1966) or "preparedness" (Seligman, 1970) ability with time. or "stimulus relevance" (Capretta, 1961) The belongingness principle in relation phenomenon—that is, the tendency to as- to taste-aversion learning is elaborated by sociate tastes with aversive internal con- Garcia and Ervin (1968) and Garciatet al. sequences as opposed to associating either (1971). Further extensions of the principle element with anything else—seems emi- to areas outside of feeding have been dis- cussed by Seligman (1970) and Shettle- nently sensible from an adaptive point of 7 view. Gastrointestinal and related internal worth (1971). events are, in fact, very likely to be in- 7 The principle of belongingness makes some pre- itiated or influenced by substances eaten, dictions about what aversive stimuli should be em- and taste receptors, by virtue of their loca- ployed in various types of aversion therapy. For tion, provide information about these same example, it would be expected that nausea-producing drugs such as apomorphine should be more effective substances. It is essential for an omnivore than electric shock in treating alcoholism. At the to have the ability to learn rapidly which present time, the data are not clear on this point (Rachman & Teasdale, 1969). The issue is com- 6J. Kalat and P. Rozin. Learned safety as an plicated because it may be the case that humans explanation for taste-aversion delay of reinforcement learn different things with electric shock or nausea gradients. In preparation. as UCSs. 472 PAUL ROZIN AND JAMES W. KALAT
Salience. There is evidence for "intra- outside of the gastrointestinal system. On modality" belongingness. Rats tend to the other hand, it is hard to understand, associate poisioning with some novel solu- from an adaptive point of view, why pain tions more than others (Kalat & Rozin, in the lungs or heart, for example, should 1970). Rats drank one novel solution be selectively associated with taste. As a briefly, 15 minutes later drank a second matter of fact, it is not known whether novel solution, and another 15 minutes gastrointestinal pain is selectively as- later were poisoned. The following day, sociated with taste. Much more research the rats were offered both solutions simul- is needed to better define the range of taneously. Under these conditions, certain visceral sensations with which tastes have solutions, which we describe as highly high associability. The extensive Russian salient, became more aversive than others. literature on interoceptive conditioning The salience of a solution proved to be a (see Bykov, 1957) demonstrates that ex- more potent predictor of amount of teroceptive cues can be attached to visceral acquired aversion than temporal proximity UCSs. Whether there is some belonging- to poisoning. It was found possible to ness operating here remains to be seen. rank novel solutions in a stable, transitive Yet another dimension of belongingness "salience" hierarchy, such that each solu- concerns the temporal parameters of the tion proved more salient (associable with various CSs and UCSs. In the taste- poisoning) than all solutions lower on the visceral system, stimuli tend to have slow list. Evidence for a salience effect on the onsets and to last for long periods. Ex- "positive" side (recovery from thiamine teroceptive CSs and UCSs, in contrast, are deficiency) has been reported (Campbell, characteristically brief and well defined in 1969). time. The importance of these dimensions As yet it is not known what constitutes and the visceral field for taste-aversion the denning characteristics of the salience learning could both be determined by using dimension. It is probable that the "rela- experimentally controlled UCSs, such as tive novelty" of these operationally novel electric shock to the stomach mucosa in- solutions contribute to the effect. By this stead of the ill-defined poisoning procedures. we mean that more salient solutions may The category of effective CSs should be more different from previously ex- differ from species to species. It was perienced solutions. There may be addi- argued above that the specific ability to tional factors associated with intrinsic prop- learn taste-poison associations is highly erties of the solutions. Certain tastes (e.g., adaptive because foods are the usual cause bitter) may have a particular tendency to of any aversive gastrointestinal stimula- be associated with aversive consequences. tion. This argument assumes that the A functional definition of belongingness, animal identifies its food by taste. How- At this time we know that some category ever, some species use other modalities of CSs, including tastes, preferentially as well. In particular, there is reason to associates with some category of UCSs, in- believe that birds put main emphasis on cluding "gastrointestinal distress." We visual cues in the identification and selec- would like to define these categories more tion of food. A number of experiments by precisely. The unconditioned stimuli em- Brower (1969) indicate that birds can ployed have been described variously as readily learn aversions to the sight of "poisoning," "nausea," and "gastrointesti- food,8 and experiments by Wilcoxon, Dra- nal upset." But the category of effective 8 One type of mimicry is based on the fact that stimuli may include stimuli not suggested many birds and some other species readily learn to by these terms. Ingested foods can cer- avoid toxic or unpalatable prey. In these cases, a tainly produce significant internal effects safe, palatable species evolves coloration similar to outside of the gastrointestinal system, and that of an unsafe or unpalatable one and thereby obtains some protection due to the predator's it is indeed possible that the primary action generalization of its learned aversion (Brower, 1969; of some of the UCSs presently employed is Rothschild, 1967; Wickler, 1968). ADAPTIVE SPECIALIZATIONS OF LEARNING 473
goin, and Krai (1971) indicate that Jap- species in which food recognition is known anese quail learn poison-based aversions to occur partly via nongustatory cues. more readily to the color (or optical For instance, frogs have specific visual cells density) than to the taste of a solution. which respond maximally to flying insects Rats and bobwhite quail were poisoned and similar stimuli (Lettvin et al., 1959). half an hour after drinking a solution The above analysis suggests that stimuli which was either blue, sour, or both blue which excite these "bug detectors' might and sour. The rats subsequently showed be more easily associated with poison than considerable aversion to the sour water, other types of visual stimuli. but none to the blue (dense) water. The quail, however, showed an aversion to LONG-DELAY LEARNING both; furthermore, the quail poisoned on blue-sour water generalized their aversion Until recently it appeared that learning to blue water and not to sour water. To of both classical and operant types was show that the aversion to blue water was almost impossible with delays of rein- not based on the taste of the blue coloring, forcement exceeding a few seconds. The the investigators showed that quail could importance of close temporal contiguity form an aversion to plain water in a dis- has been demonstrated in a considerable tinctively colored tube. variety of experimental paradigims, and We suggest that the critical dimension apparent exceptions seemed to depend on for poison-based aversion learning may secondary reinforcement (Kimble, 1961). not be "taste versus other modalities" but There were cogent theoretical and adaptive "eating-related cues versus other cues." reasons for assuming the universal im- This type of functional categorization of portance of close temporal continguity. input is in harmony with Gibson's (1966) Premonitions existed, however, of a pos- view of perceptual systems. Eating-related sible problem with learning about food cues would be whatever type of cue— ingestion. gustatory, visual, or otherwise—a particu- History lar species uses to identify food. Because of the intimate and relatively invariant The first such reference is Pavlov (1927). relationship between taste receptors and Using morphine as a UCS, Pavlov noted food ingestion, and because of the neuro- signs of nausea and profuse salivation in logical association between taste and vis- response to the touch of the experimenter, ceral receptors, it is likely that taste cues which preceded injection. Needless to say, would always be classified as eating- the UCS (i.e., nausea, etc.) did not occur related so that taste-poisoning belonging- until many minutes after the morphine was ness should be practically universal. How- administered. Pavlov evidently regarded ever, in some species, other modalities the effect as a species of conditioning, thus may also be eating related. implicitly accepting the possibility of Nontaste sensory modalities could in- learning over long delays: clude both eating-related and non-eating- This experiment provides a clue to the well-known related cues. For instance, it may be that fact that dogs will eat meat the first time it is birds can form poison-based aversions to offered them, after removal of their parathyroids, or the sight of potential prey, but not to after an Eck fistula and tying of the portal vein, but other sights. Also, it is known that odors on all subsequent occasions will refuse it. Evidently in these cases the appearance and smell of meat are less effective than tastes in poison- produce of themselves a reaction identical with that based aversions in rats. Possibly odors produced through direct pathological action in the are more effective when they emanate from absence of the parathyroids or the portal circulation, a food source or if they are experienced by those toxic substances resulting from digestion of simultaneously with a taste. It would be the meat [p. 36]. interesting to investigate the effective cues A similar recognition of the phenomenon for poison-based aversion learning in other of long-delay learning is present in the 474 PAUL ROZIN AND JAMES W. KALAT biological literature on poisoning, regula- one hour. Smith and Roll (1967) found tion of food intake, and specific hungers. similar results using X rays and either Thus, Harris et al. (1933), Scott and saccharin (up to 12-hour delays) or sucrose Verney (1947), Rzoska (1953), and Le- (up to 6-hour delays). Replications by Magnen (1969) explicitly implicated learn- Revusky (1968) using sucrose CS and ing mechanisms; to biologists without any X-ray UCS and Rozin (1969b) (using particular commitments to psychological saccharin or casein hydrolysate as CSs and theory, this explanation seemed perfectly apomorphine as UCS) confirmed this effect. plausible. One way of reconciling these data to Hypotheses to Explain the Long Delay traditional S-R learning theory was to Peripheral—the aftertaste theory. Be- assume that animals associated a food with cause of the revolutionary nature of this the consequences of a previous meal of the finding, there was considerable interest in same food, thus achieving temporal con- the possibility that the apparent absence of tiguity (Rozin et al., 1964; Smith & temporal contiguity was illusory. Although Capretta, 1956). But rats need only a the CS-UCS interval was ostensibly long, single exposure to a toxic food to learn to some peripheral trace of the CS might re- avoid it (Rzoska, 1953); thus some other main throughout the interval in the form explanation is necessary. of an aftertaste, regurgitation, or a high The discovery that long CS-UCS in- concentration in the blood. It could be tervals are possible in learning about the this trace that was involved in the condi- consequences of foods occurred gradually. tioning. However, a fair amount of data Garcia et al. (1961) in their early work are now available to oppose this explana- found that rats learned food aversions on tion. The main import of the data is that the basis of simultaneous exposure to X taste-aversion learning is possible under rays. Although it was known that X rays conditions that should greatly minimize had their main effect with a considerable any aftertaste. delay ("radiation sickness"), it was as- First, taste-aversion learning to sucrose sumed that some immediate effect of X and saccharin solutions occurs on a single rays was involved in the learning, and trial with maximum delays of poisoning slight evidence was offered to support this of about 7 and 12 hours, respectively position. McLaurin (1964) was the first (Revusky, 1968; Smith & Roll, 1967). It to operationally manipulate CS-UCS inter- is very doubtful that an aftertaste or vals over a wide range in taste-aversion perceptible change in blood concentration learning with long delays of reinforcement. persists for such long periods. It is even However, a methodological flaw precluded less plausible to suggest that enough meaningful interpretation of this result; sucrose or saccharin remains in the stomach McLaurin tested for aversion immediately at this time to be tasted by regurgitation. after exposure to X rays, and it was later Actually the regurgitation model never demonstrated (Smith & Schaeffer, 1967) had much applicability to rats anyway, that the rats were learning aversions to the since rats rarely if ever vomit. A second test solution during the test itself. That argument against the aftertaste and re- is, the drinking of the solution during lated models is the fact that rats can learn testing was simultaneous with the develop- aversions to a .05% HC1 solution with a ment of aversive consequences of the one-hour delay of reinforcement (Garcia, X rays, and temporal contiguity was Green, & McGowan, 1969). A litmus achieved. Garcia et al. (1966) avoided paper test showed no measurable amount this problem by giving the test for sac- of HC1 on the tongue two minutes after charin aversion three days after exposure the animal stopped drinking. Thus, the to apomorphine. This experiment suc- likelihood of a conventional peripheral cessfully demonstrated learning with long aftertaste an hour later is minimal. Fur- delays of reinforcement of the order of thermore, the solution was less concentrated ADAPTIVE SPECIALIZATIONS OF LEARNING 475 than the HC1 already in the stomach. aversions would not solve the delay prob- Consequently, this experiment is peculiarly lem, as the HC1 experiments (Garcia et al., effective in eliminating regurgitation, stom- 1969), concentration aversions (Rozin, ach-tasting, and blood-tasting models. A 1969b), and solution temperature aversions third line of evidence is Rozin's (1969b) (Nachman, 1970a) are no easier to explain demonstration that rats can learn an in terms of contiguity with intragastric aversion to a specific concentration of a stimuli. solution as opposed to other concentra- Bradley and Mistretta (1971) have tions of the same solution. The animal demonstrated the development of aversions learned the aversion just as easily to the to intravenously introduced solutions (sac- lower as to the higher concentration. Pre- charin) in rats, using X rays as the UCS. sumably after the 30-minute delay used in A circulating "slug" of high-concentration this experiment, the aftertaste of a more saccharin stimulates taste receptors in the concentrated solution should taste more tongue. This interesting experiment pro- like a less concentrated solution of the vides another mechanism of learned aver- same substance. Similarly, the blood or sions, but it cannot be the only mechanism stomach concentration of the substance at involved in orally mediated aversions. the time of poisoning should not be uniquely The blood concentrations used in these related to a particular concentration of experiments are much higher than any original solution by a function known in- which would occur naturally or in the dependently by the rats. A fourth line long-delay experiments, and the same ex- of evidence is Nachman's (1970a) demon- periments discussed above as raising prob- stration that rats can learn an aversion to lems for an intragastric-tasting mechanism a particular temperature of water; an would be equally troublesome for a "blood- aftertaste of a temperature is difficult to tasting mechanism." imagine. Fifth, rats can learn an aversion At present there is no evidence in favor to a solution even if one or more solutions of an aftertaste theory and a considerable is drunk between the first solution and body of evidence against it. Establish- poisoning (Kalat & Rozin, 1970, 1971a; ment of an alternative theory seems a more Revusky & Bedarf, 1967). The interven- appropriate strategy than accumulation ing solutions would surely minimize any of still further evidence against aftertaste aftertaste of the first. Finally, it has been interpretations. Of course, from the point argued (Revusky & Garcia, 1970) that of view of this paper, long-delay learning even if the aftertaste model were correct, is exactly what should be expected in this it would be difficult to reconcile the taste- situation, and the central-mediation alter- aversion learning results to conventional native appears quite acceptable. learning theories. Even if there is an Central mechanisms—interference. Re- aftertaste, it would have been present and vusky (in press; see also Revusky & declining in intensity for such a long Garcia, 1970) proposes that the maximum period that there would be no precedent CS-UCS interval in all types of learning for expecting learning to occur—let alone depends not on time per se, but on the in one trial. number of other potential CSs that in- It may be argued that none of these tervene between the^CS being tested and arguments completely demolishes an after- the UCS. That is, the animal tends to taste theory, and that certain other tests associate the UCS with the most recent could be conducted, for example, attempt- potential CS, or perhaps the last several ing to produce aversions to solutions such stimuli. As the CS-UCS interval intubated intragastrically. Some recent expands, the probability increases that the evidence suggests that if such aversions organism will perceive other sights, sounds, occur at all, they are much smaller than etc., and consequently the probability de- taste-mediated aversions (Smith, 1970). creases that the animal will associate the However, even if demonstrable, intragastric UCS with the CS in question. In taste- 476 PAUL ROZIN AND JAMES W. KALAT
aversion learning, the argument holds, the novel solutions during a 30-minute delay range of potential CSs is much more re- between sucrose consumption and poison stricted. Only tastes have a substantial does not eliminate the sucrose aversion tendency to be associated with aversive (Kalat & Rozin, 1971a). The maximal gastrointestinal stimulation, and typically interference effect we observed using three the test solution is the most recent taste novel interfering solutions following sucrose, the animal experienced prior to poisoning. and one poisoning, left sucrose equally Since no other potential CSs are present, palatable with water, to which it is normally there is nothing to interfere with learning strongly preferred. over long delays. In taste aversion as in These experiments, then, suggest that other learning, the animal tends to as- retroactive interference can clearly weaken sociate a UCS with the last potential CS; a potential association, but it is highly the only difference is that in taste-aversion unlikely that the normal delay function can learning, the potential CSs are fewer and be largely accounted for in these terms: less frequent. We would like to point out What could interfere with drinking of a test that the taste modality differs from the solution during six hours of no eating or commonly studied exteroceptive modalities, drinking that would be more effective than in that virtually all stimulation comes from three novel solutions? Proactive interfer- contacts initiated by behavior. Rats do ence is an unlikely explanation. Effects not taste unless they approach something from past taste experiences should be and introduce it into their mouth. minimal, since most rats have experienced This theory is very attractive because only highly familiar rat chow, water, and it proposes that the differences between mother's milk. taste-aversion learning and other types Recent findings by Wilcoxon et al. of learning may all be derived from the (1971) pose further problems for Revusky's general principle of belongingness, without theory. Unlike rats, bobwhite quail poi- postulating an independent difference in soned 30 minutes, after drinking unflavored the delay of reinforcement function. water from a blue tube learn an aversion Nevertheless, the theory, if taken as the to drinking from that tube. Since the sole^of primary explanation of delay, faces quail presumably saw a great many visual two serious problems. It predicts that in stimuli in the 30-minute delay, their the absence of interfering taste cues, there ability to learn over long delays in this should be little or no decrement in learning situation cannot be explained simply in as the CS-UCS interval is increased. This terms of absence of interference. is not the case. Garcia et al. (1966), Although it seems unlikely that inter- Nachman, (1970a), Revusky (1968), and ference represents the only basis for the Kalat and Rozin (197 la) have all found CS-UCS delay gradient, it does appear to an orderly decrease of aversion with in- be a contributing factor. Since a rat creasing CS-UCS interval. Furthermore, normally experiences fewer tastes than all experiments have found a maximal other stimuli within a given period, the interval, varying from about 2 to 12 hours, Revusky theory may account for part of beyond which no learned aversion can be the difference in the delay gradients be- demonstrated. Kalat and Rozin (197la) tween taste-aversion and other types of deprived rats of both food and water during learning. the CS-UCS interval, and still observed Slow decay of associability as an inherent an orderly decrease in learned aversions property of the taste system. An alternative with increasing CS-UCS interval. to the view that the delay-of-reinforce- Not only is there a decrement in learn- ment gradient is a function of interference ing in the absence of explicit interference, is the view that the delay gradient is an but the addition of explicit interfering cues inherent property of the system itself; does not markedly reduce learning. The memory or associability decays much consumption of two or even three salient more slowly for taste than for other ADAPTIVE SPECIALIZATIONS OF LEARNING 477
modalities. This leaves unanswered the tastes remain in short-term memory for a question, What accounts for this decay? long time. One possibility is that the delay func- Another possible mechanism for the delay tion represents the decay of short-term function is that some central long-term memory. According to this hypothesis, a "trace" of the taste is decaying over time. stimulus is associable with other events Unfortunately, this is a difficult hypothesis only while it is held in short-term memory, to test. One experiment (Rozin & Ree9) and tastes remain in short-term memory at least puts certain constraints on the for unusually long periods. (Although type of decay which is possible. Rats there is extensive data on short-term were anesthetized for 6-8 hours during the memory in humans, virtually none has interval between consumption of a sucrose been collected on taste, and it is con- solution and LiCl poisoning. These rats ceivable that tastes do not compete with showed strong learned aversions at delays exteroceptive cues for space in short-term of poisoning considerably longer than those memory.) which are effective in the absence of One way of testing this hypothesis is by anesthesia. Thus anesthesia seems to means of electroconvulsive shock, which retard whatever process mediates the has been assumed to eradicate short-term delay of reinforcement gradient. If this memories or to block their conversion to process is to be described as "decay," it is long-term memories. If taste associations evidently an active rather than a passive must be made from short-term memory type. extended in time, it should be possible to Central mechanisms—learned safety. The demonstrate disruptive effects of electro- suggestion of an "active decay" process convulsive shock, presented within the raises still another possibility, which is not CS-UCS interval but with longer delays a decay mechanism at all. Perhaps the following the CS than are ordinarily delay gradient should be viewed not as a effective in disrupting other types of forgetting curve but as a learning curve. memory. In a very careful study, Nach- That is, in the absence of unfavorable man (1970b) found amnesic effects of gastrointestinal events, as time passes electroconvulsive shock in some rats when .following consumption of a novel solution, electroconvulsive shock was presented im- the animal learns that the solution is safe mediately after 10 seconds of drinking but (Kalat & Rozin, see Footnote 6). not after 30 seconds of drinking. He also As evidence for this, it has been demon- found some amnesic effects from electro- strated that an animal does learn some- convulsive shock presented 25 seconds thing about a solution when consumption after a 5-second drinking period. Krai of that solution is followed by no negative (1970) also found small amnesic effects consequences. We have already discussed with electroconvulsive shock, using delays the evidence indicating that rats learn less of 2 or 25 minutes following a 10-minute aversion to familiar solutions than to novel drinking period. As is usual with elec- solutions (Revusky & Bedarf, 1967) even troconvulsive shock experiments, the tem- when the familiar solution was experienced poral parameters seem to vary widely from once for only 20 minutes, three weeks one experiment to another. However, in both cases, the effect of electroconvulsive before poisoning (Kalat & Rozin, see shock is small; it impeded but did not Footnote 6). This interpretation goes on prevent learning. And in both cases, the to make a stronger claim: The learning of effective electroconvulsive shock times were "safety" takes place within the period within the range of times reported for measured by the maximum delay of electroconvulsive-shock-amnesic effects in reinforcement. At the end of that period, other systems. Thus there is no evidence 9 P. Rozin and P. Ree. Long extension of effective that the transfer of taste stimuli into long- CS-UCS interval by anesthesia between CS and US. term memory is unusually slow, or that In preparation. 478 PAUL ROZIN AND JAMES W. KALAT the "trace" has not decayed; it has merely What Kind of Learning Is This ? been associated with the absence of aversive consequences. At intermediate delays, the We have already described a number of intermediate amount of learned aversion differences between taste-aversion learn- reflects the fact that the animal has ing and traditional learning. We shall now learned an intermediate amount of safety. consider some additional evidence in order Although this interpretation is grossly to determine how fundamental this dis- different (and not inconsistent with) the tinction is. Recent experiments have interference or trace-decay interpretations, suggested two additional differences. First, it is not easy to separate the alternatives it appears that rats can learn taste aver- sions when poisoned under anesthesia experimentally. The results of Rozin and (Berger10; Roll & Smith, in press). Anes- Ree (see Footnote 9), which suggest that thesia was continued for a long period fol- indefinitely long CS-UCS intervals will lowing UCS administration, so that it was support aversion learning if the rat is highly likely that the learning occurred anesthetized during the interval, are con- under anesthesia. Second, one of the more sistent with learned safety, since it is "complex" characteristics of classical con- reasonable that the rat would be unable to ditioning, the Kamin blocking effect (Ka- learn safety while anesthetized. min, 1969), is either nonexistent or rela- tively weak in taste-aversion learning WHAT ALL THIS MEANS TO THE RAT (Kalat & Rozin, 197Ib; Revusky, in press). We are now prepared to describe how a One interpretation of why taste-aversion rat can handle some of the complex prob- learning does not clearly show the Kamin- lems in food selection. The first thing to type effects is that the taste does not be- realize is that the situation is probably less come a signal for poison in the sense that complex than it might appear when the a tone or light becomes a signal for shock. rat's natural behavior is considered. For In taste-aversion learning, the animal's example, the rat who gets sick in the gar- perception of the taste itself or of its bage dump probably did not recently affective value may change (suggested by sample all the choice delicacies available H. Gleitman, personal communication, (Rozin, 1969a). His choice behavior 1971). The taste itself may become itself will help to unconfound the situation. aversive or unacceptable, as if it were un- He may have eaten a few different foods. palatable (Rozin, 1967b). By contrast, He "knows" it was & food that made him stimuli associated with shock do not them- sick (the belongingness principle) and selves become aversive; they evoke little can discount any familiar safe foods (the avoidance outside the training situation. novelty principle). With the capability This difference seems related to the re- of forming associations over long delays, ported "irrationality" of learned taste he is now likely to associate his illness aversions; humans commonly maintain with the last relevant (as defined above) an aversion to foods they ate prior to thing or few things he ate over the last becoming nauseous, even when they are few hours. Although some of these foods sure that some other agent was responsible may become more aversive than others be- for the nausea. cause of their intrinsic properties (salience Seligman (1970) has suggested that effect), the rat will acquire a significant taste-aversion learning may be a particu- aversion to each of them (small inter- larly primitive type of learning. The ference effect), with those closer in time evidence mentioned above is quite con- to the aversive event picking up somewhat sistent with this view. Furthermore, in a more aversion (temporal contiguity). Simi- biological context, it makes sense that this lar mechanisms would be employed to ability should be primitive. The problems account for important aspects of the regula- 10 B. Berger. Learning in the anesthetized rat. 1ion of food intake. In preparation. ADAPTIVE SPECIALIZATIONS OF LEARNING 479 of food selection and the regulation of food perform just that function. How specifically these intake are pervasive ones, and both are mechanisms are differentiated for one particular function is borne out by the fact that they are very likely to involve long-delay learning. The often quite unable to modify any but one strictly essential problems are relatively invariant determined system of behavior mechanisms fJLorenz, across species: any new food has some 1965, p. 47]. probability of being toxic, and for almost We are aware of only two well-studied all species, the caloric density of foods will systems showing adaptive specializations of vary. Therefore, it makes sense that taste learning. One is feeding, which we have aversion and related types of learning already discussed, and the other involves should be more or less the same throughout imprinting, as a mechanism of species most of the vertebrate subphylum. recognition. Two of the prominent features of im- ADAPTIVE SPECIALIZATIONS OF LEARNING: printing—the special sensitivity during a GENERALITY AND RELATION TO critical period early in life and the great OTHER POSITIONS resistance to extinction—can be seen as The work on specific hungers and poi- adaptations to limit the likelihood of soning suggests that there are two aspects errors in species recognition. The learning of adaptive specializations of learning. should take place soon after hatching, since First, some mechanisms of learning may the probability of exposure to a conspecific differ markedly (at least in terms of large (i.e., the mother) is highest at this time, quantitative differences in basic parameters) and the bird should be less sensitive to in the feeding system, as compared to other later experiences, since the frequency of systems. Second, understanding of an contact with members of other species is adaptive specialization includes delimita- likely to increase greatly after the nestling tion of the situations in which it applies period. and elaboration of its relationship and Feeding and imprinting can be con- interaction with the animals' natural be- sidered as two exceptions to an otherwise havior (e.g., sampling, neophobia) in the correct "general process" view of learning, relevant situation. The variation in inter- or they can be considered as examples play among naturalistic context, genetic of a basic adaptational principle pervading programming, and learning is clearly il- much or all of learning. We prefer the lustrated in the contrast between water latter alternative and believe that the or sodium hunger, and other specific absence of additional known instances of hungers. adaptive specializations may reflect learn- Our emphasis has been on the first aspect ing psychologists' reluctance to study of adaptation, while the ethologists have potentially learned behaviors which do not focused more on the context of learning fit into the general process paradigms. and interplay of prestructured and ac- (Significantly, the case for adaptive spe- quired components: cializations in both imprinting and feeding came from outside the psychology of The student of innate behavior, accustomed to learning.) studying a number of different species and the entire behavior pattern, is repeatedly confronted with the At this point one can only speculate fact that an animal may learn some things much about what other systems will show special more readily than others. ... In other words, adaptations of learning. Bees may possess there seem to be more or less strictly localized a wide variety of adaptive specializations "dispositions to learn." Different species are pre- (von Frisch, 1953, 1967). A particularly disposed to learn different parts of the pattern. So far as we know, these differences between species promising example is their navigational have adaptive significance [Tinbergen, 1951, p. 145]. ability. First, there is evidence for "belongingness." . . . innumerable observations and experiments tend to show that modifiability occurs, if at all, only Honey bees can learn to^use irregular forms, like in those performed places where built-in learning those of trees or rocks, as landmarks by which to mechanisms are phylogenetically programmed to steer a course to and from the hive; but they cannot, 480 PAUL ROZIN AND JAMES W. KALAT even by the most subtle conditioning technique, be not been thoroughly studied as possible taught to use the same forms as positive or negative signals indicating the presence or absence of food in specialized learning mechanisms. a tray, as von Frisch (1914) has shown. As signals The "heuristic" value of an adaptive for food, bees can distinguish different forms only if evolutionary point of view can be suggested they are geometrically regular, preferably radially by considering the types of predictions symmetrical (Hertz, 1937) [Lorenz, 1965, p. 47]. that might be made about some basic Second, a limited amount of experience in learning and memory relationships. For observing a piece of the sun's arc enables example, an organism's memory of some the bee to "project" the rest of the arc. aspect of the environment is useful only That is, bees raised without the oppor- if that aspect is predictable or controllable; tunity to see the sun have great difficulty otherwise, rapid forgetting might be ad- compensating for sun movement during vantageous. It is probably of no use for navigation. But bees that have observed bees, birds, or other organisms with com- sun movement only during a limited period plex navigational abilities to remember in the morning are fully capable of com- whether it was cloudy yesterday or which pensating for sun movement in the after- way the wind was blowing, though both noon (von Frisch, 1967). In this situa- may have been important at the time. tion, the environmental input produces a Under these circumstances one might long-term change, and does not act "as- expect to find a specialization in short- sociatively," but rather provides a refer- term memory such that information could ence point. Other examples of such be stored for longer periods and in greater "calibrational learning" (Lorenz, 1965) quantities than usual without entering might include adaptation to visual dis- long-term memory. placement produced by prisms and caloric Another example concerns extinction. regulation.11 Extinction, from an adaptive point of The naturalistic literature is replete with view, allows an organism (a) to correct for other examples of surprising abilities of mistakes (fortuitous conditioning) and (b) animals—such as digger wasps' memory of to constantly reshape itself to adapt to a the location and state of their nests variable environment. One might expect (Baerends, 1941), gobies' latent learning the rapidity of extinction to depend on the of the location of tidepools (Aronson, probability that either of these events 1951), salmon's recognition of home-stream would occur. In the case of imprinting, we odor (Hasler, 1966), doves' individual mate have great resistance to extinction in a recognition (Morris & Erickson, 1971), case where clearly the environment will sparrows' acquisition and storage of song not vary (i.e., the species will not change), dialects (Marler, 1970), etc. These have and the proper imprinting object is almost certain to be present at the time of im- 11 We can suggest a role for "calibrational learn- ing" in the regulation of food intake. It has been printing. The great resistance to extinc- known for some time that rats and other mammals tion of avoidance conditioning (Solomon & respond to changes in caloric density of food by Wynne, 1954) may be an adaptively appropriate modulation of volume intake. In the selected feature of this learning: the costs rat, this compensation occurs largely as an increase of errors of omission here are high. One in meal size, rather than in number of meals (Snowdon, 1969; Teitelbaum & Campbell, 1958). might expect rapid extinction of the When a standard diet is diluted, the rat ends up learned location and stimulus properties eating larger meals: he has "recalibrated" his meal of food sources, where these sources are size on the basis of the metabolic aftereffects of his subject to marked seasonal or other tem- meals. It is possible to imagine a mechanism which compares some measure of the amount ingested with poral variations. An example might be its delayed metabolic effects, and adjusts future extinction of responses to particular types intake downward or upward so that the metabolic and locations of flowers in foraging bees. consequences will approach some preferred or ideal One might observe slow learning, but high value. The demonstration of a long-delay learning mechanism makes this type of explanation feasible resistance to extinction in a situation where and subject to investigation. the environment is stable but a critical ADAPTIVE SPECIALIZATIONS OF LEARNING 481 difference is relatively hard to detect More significantly, the long-delay learning (e.g., prey density), and "averaging" must found in feeding is probably not character- be done before a clear choice or preference istic of other "prepared" associations, and is established. One might observe rapid in our view, it should not be, since in most learning and rapid extinction in a rapidly cases close temporal contiguity is the best changing environment (see Shettleworth, predictor. Furthermore, we see no reason 1971, for additional comments on this to expect a consistent relationship between point). rapid learning and high resistance to ex- Recently, a number of authors have ex- tinction (see discussion of extinction above). pressed positions related to ours (Garcia & In short, we disagree with Seligman that Ervin, 1968; Garcia et al., 1971; Revusky, diversity can be ordered along any single, in press; Revusky & Garcia, 1970; Selig- operationally meaningful dimension, that man, 1970). We differ from all of these is, preparedness. If preparedness meant authors in the sense that they see be- adaptedness to situational demands, it longingness, in one form or another, as would be an acceptable but not clearly the unique phenomenon to be explained, meaningful dimension. Seligman has given whereas we see it as an example of the it operational meaning, but narrowed the general adaptational principle; animals scope of the phenomena he can account for may not only learn some things more in the process. In a more recent statement easily than others, but they may also of the preparedness position, Seligman and learn some things in a different way than Hager (in press) have acknowledged some others. The contrast is clearest in the of these possible limitations. case of Revusky, who attempts to pre- Shettleworth (1971), in a paper written serve traditional learning theory intact, concurrently with this one, has presented with the introduction of a new "belonging- a position very similar to ours. It focuses ness" assumption. on belongingness, broadly conceived, but Seligman (1970) proposes a new di- also describes learning in general in terms mension, "preparedness," based on the of adaptive specializations, and provides belongingness relationship, to incorporate examples from the naturalistic literature. recent findings into a more viable learning A recent paper by Lockard (1971) also theory. Preparedness represents the tend- explicitly discusses the diversity of learn- ency of certain inputs (and/or outputs) to ing mechanisms as an important feature be associated with one another, this ignored by most psychologists and implies tendency resulting from natural selection. that the search for common elements in Seligman proposes that highly prepared learning across species and situations is associations are established with a minimal almost hopeless. input (e.g., number of pairings). In We differ slightly from Shettleworth and addition to very rapid learning, prepared markedly from Lockard with respect to associations would tend to show learning our optimism about the possibility of find- with long delays of reinforcement and per- ing order within the diversity of learning haps high resistance to extinction. We are certainly in accord with the general mechanisms. Given the constraints on flavor of Seligman's position, but we feel adaptations produced by basic properties that in his desire to reorder the phenomena of the nervous system, the cost of evolving of learning, he has not fully appreciated specializations, and the fact that most the diverse natural forces that can shape species face a common set of problems, we behavior and learning mechanisms. In doubt that a separate learning mechanism imprinting, for example, wh£re Seligman's would exist for every situation, or that view of rapid learning (and high resistance there would be separate laws for each to extinction) fits very wellj the presence species. It may yet be possible to formu- of the critical period canntot be accom- late laws of some degree of generality, modated without additional assumptions. taking ecological factors into account (see 482 PAUL ROZIN AND JAMES W. KALAT
Walls, 1942, for an example in the area of certain higher learning abilities that "fish" vision). do not possess. Another not mutually ex- clusive possibility is that the rat and SOME SPECULATIONS probably most other mammals are "gen- It follows from the point of view pre- eralists," compared to the majority of other sented here that an organism may have an vertebrates. That is, abilities initially ability that manifests itself in only a small evolved to handle a specific situation and number of the total possible situations in limited in application to the appropriate which an experimenter might test for it. system may turn out to be useful in others The ability in question might be inac- and may through evolution be "connected" cessible to or "unconnected" with the into new systems. To what extent do the machinery for modulating and controlling higher abilities of the mammals represent most behavior. Using a computer analogy, an increase in accessibility of specialized we might suppose that a particular routine capacities, an "emancipation," to borrow is designed (evolved) to handle a specific a word from the ethologists, of a capacity problem. At this point in time, it is from its original tight motivational system ? physically connected only into the relevant The proposed increase in accessibility of inputs, outputs, or systems, and is in- capacities in phylogeny may have a par- accessible to the rest. Under these cir- allel in ontogeny. Within the Piagetian cumstances, it would be difficult to describe framework, it is apparent that particular a species' learning capacity. cognitive structures may have only limited The interesting demonstrations by Bit- applicability at any point in development. terman (1968), Gonzalez and Bitterman Piaget applies the name "decalage" to this (1969), and Mackintosh (1965) of dif- feature of development. (Flavell, 1963, ferences in learning abilities in certain pp. 21-24). For example, in the Piagetian situations between a few species of fish scheme, the same cognitive structure is and mammals do not in themselves in- necessary for the achievement of mass and dicate complete absence of these abilities weight conservation, yet the latter occurs in any species of fish (see Gleitman & about two years after the former. Cogni- Rozin, in press, for a general review of this tive development may consist, in part, of issue with respect to learning and memory the extension of existent capacities to new in fish). A species should be tested for situations, in parallel to our scheme for any ability in those situations where its phylogeny. existence would have the greatest survival We have argued for the existence of value. The failure of a few fish species to adaptive specializations in learning and demonstrate abilities such as progressive memory. Since, by their nature, such improvement in habit reversal in a few specializations are limited to a relatively laboratory situations does not meet this narrow range of situations, we have pointed demand. out that they must be inaccessible to most However, the data gathered by Bitter- functioning systems. We believe that this man, by Gonzalez and Bitterman, and by general formulation has a wide application, Mackintosh do suggest some interesting and we are presently applying it to an phylogenetic generalizations about learn- understanding of the difficulties in initial ing capacities. Since the laboratory ap- acquisition of reading (Rozin & Kalat, paratus used to study rats and other in press; Rozin, Poritsky, & Sotsky, 1971). mammals is often not ideally suited to It is the basic thesis of this paper that in their natural behavior, just as the fish a biological-evolutionary framework, spe- apparatus is not, it is quite interesting that cifically adapted abilities are extremely mammals reliably show the greater plas- important and should not suffer from ticity in these "unnatural" situations. One neglect as a consequence of the search for possible explanation for this, offered by great generalities. To understand a set Bitterman (1964), is that the rat possesses of phenomena, within humans or across ADAPTIVE SPECIALIZATIONS OF LEARNING 483
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